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Westminster began as a gathering of eight people of Scottish, Irish and Welsh heritage in 1857. In 1860, the congregation built its first church, on Fourth Street between Nicollet and Hennepin Avenues in downtown Minneapolis. Because of the rapid growth of the congregation, the church soon outgrew its first location. In 1883, construction of a new, larger church began at Seventh Street and Nicollet Avenue.

Twelve years after the opening of the second church site, the building was heavily damaged by a fire. This prompted yet another move when the church rebuilt to its current location at Twelfth Street and Nicollet Mall, opening its doors for services in 1897.

In 1998, to coincide with the building's centennial, the congregation undertook an extensive renovation of the sanctuary. This 3.5 million dollar project restored many of the sanctuary's original design elements, updated the structure and improved lighting and sound. The newly renovated sanctuary opened for services on Sunday, December 20, 1998.